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Wolbachia is not all about sex: male-feminizing Wolbachia alters the leafhopper Zyginidia pullula transcriptome in a mainly sex-independent manner.

Asgharian H, Chang PL, Mazzoglio PJ, Negri I - Front Microbiol (2014)

Bottom Line: Despite the resemblance of Wolbachia-infected chromosomal males to uninfected and infected chromosomal females in terms of sexual morphology and behavior, principal component analysis revealed that gene expression patterns did not follow these sexual phenotype categories.The principal components generated by differentially expressed genes specified a strong sex-independent Wolbachia effect, followed by a weaker Wolbachia-sexual karyotype interaction effect.Approaches to further examine the molecular mechanism of Wolbachia-host interactions have been suggested based on the presented findings.

View Article: PubMed Central - PubMed

Affiliation: Program in Molecular and Computational Biology, Department of Biological Sciences, University of Southern California Los Angeles, CA, USA.

ABSTRACT
Wolbachia causes the feminization of chromosomally male embryos in several species of crustaceans and insects, including the leafhopper Zyginidia pullula. In contrast to the relatively well-established ecological aspects of male feminization (e.g., sex ratio distortion and its consequences), the underlying molecular mechanisms remain understudied and unclear. We embarked on an exploratory study to investigate the extent and nature of Wolbachia's effect on gene expression pattern in Z. pullula. We sequenced whole transcriptomes from Wolbachia-infected and uninfected adults. 18147 loci were assembled de novo, including homologs of several Drosophila sex determination genes. A number of transcripts were flagged as candidate Wolbachia sequences. Despite the resemblance of Wolbachia-infected chromosomal males to uninfected and infected chromosomal females in terms of sexual morphology and behavior, principal component analysis revealed that gene expression patterns did not follow these sexual phenotype categories. The principal components generated by differentially expressed genes specified a strong sex-independent Wolbachia effect, followed by a weaker Wolbachia-sexual karyotype interaction effect. Approaches to further examine the molecular mechanism of Wolbachia-host interactions have been suggested based on the presented findings.

No MeSH data available.


Related in: MedlinePlus

Principal component analysis of gene expression levels in four Zyginidia samples: infected females (FW), infected males or intersex females (MW), uninfected females (F) and uninfected males (M). The first three PCs are depicted here. PC1 is correlated with all sample labels but PC2 separates the infected and uninfected samples conclusively. PC3 reveals an interaction term between Wolbachia status and sexual karyotype. The “_ql” suffix after line names means that the expression values were quantile-normalized and log transformed. (A) PC1 vs. PC2; (B) PC1 vs. PC3.
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Figure 2: Principal component analysis of gene expression levels in four Zyginidia samples: infected females (FW), infected males or intersex females (MW), uninfected females (F) and uninfected males (M). The first three PCs are depicted here. PC1 is correlated with all sample labels but PC2 separates the infected and uninfected samples conclusively. PC3 reveals an interaction term between Wolbachia status and sexual karyotype. The “_ql” suffix after line names means that the expression values were quantile-normalized and log transformed. (A) PC1 vs. PC2; (B) PC1 vs. PC3.

Mentions: Principal component analysis on transcriptomes of the four leafhopper samples surprisingly revealed that Wolbachia infection changes the host transcriptome extensively and the effect is by no means limited to sex-reversal. As evident in Figure 2, the first PC (explaining 66.46% of variance) is highly correlated with all of the samples indicating that the expression of most genes is not significantly altered by Wolbachia and is similar across all samples. By the second PC (explaining 20.36% of variance), Wolbachia infected male and female samples cluster together and uninfected male and female cluster together. This PC is generated by genes whose expression is changed by Wolbachia consistently regardless of sexual karyotype or phenotype. The third PC (explaining 7.97% of variance) indicates an interaction term: F and M are similar and stand in the middle of the scale, with MW and FW occupying the opposite sides of them. This PC is generated by genes that are expressed similarly in uninfected males and females, and Wolbachia infection changes their expression in opposite ways in chromosomal males and females. Overall, sex inversion does not seem to be the only or even the biggest effect of Wolbachia on gene expression patterns in Zyginidia, even if it is the most conspicuous phenotypic consequence; otherwise, we would expect the three phenotypically female groups (F, FW and MW) to cluster together and the only male group (M) to stand separate from them. None of the PCs show such a pattern. PCA was repeated on expression values without the initial outlier filtering, and applying several different normalization and transformation strategies; they all yielded the same picture as described above: the main effect was invariably the presence or absence of Wolbachia regardless of sex (details not shown).


Wolbachia is not all about sex: male-feminizing Wolbachia alters the leafhopper Zyginidia pullula transcriptome in a mainly sex-independent manner.

Asgharian H, Chang PL, Mazzoglio PJ, Negri I - Front Microbiol (2014)

Principal component analysis of gene expression levels in four Zyginidia samples: infected females (FW), infected males or intersex females (MW), uninfected females (F) and uninfected males (M). The first three PCs are depicted here. PC1 is correlated with all sample labels but PC2 separates the infected and uninfected samples conclusively. PC3 reveals an interaction term between Wolbachia status and sexual karyotype. The “_ql” suffix after line names means that the expression values were quantile-normalized and log transformed. (A) PC1 vs. PC2; (B) PC1 vs. PC3.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4150536&req=5

Figure 2: Principal component analysis of gene expression levels in four Zyginidia samples: infected females (FW), infected males or intersex females (MW), uninfected females (F) and uninfected males (M). The first three PCs are depicted here. PC1 is correlated with all sample labels but PC2 separates the infected and uninfected samples conclusively. PC3 reveals an interaction term between Wolbachia status and sexual karyotype. The “_ql” suffix after line names means that the expression values were quantile-normalized and log transformed. (A) PC1 vs. PC2; (B) PC1 vs. PC3.
Mentions: Principal component analysis on transcriptomes of the four leafhopper samples surprisingly revealed that Wolbachia infection changes the host transcriptome extensively and the effect is by no means limited to sex-reversal. As evident in Figure 2, the first PC (explaining 66.46% of variance) is highly correlated with all of the samples indicating that the expression of most genes is not significantly altered by Wolbachia and is similar across all samples. By the second PC (explaining 20.36% of variance), Wolbachia infected male and female samples cluster together and uninfected male and female cluster together. This PC is generated by genes whose expression is changed by Wolbachia consistently regardless of sexual karyotype or phenotype. The third PC (explaining 7.97% of variance) indicates an interaction term: F and M are similar and stand in the middle of the scale, with MW and FW occupying the opposite sides of them. This PC is generated by genes that are expressed similarly in uninfected males and females, and Wolbachia infection changes their expression in opposite ways in chromosomal males and females. Overall, sex inversion does not seem to be the only or even the biggest effect of Wolbachia on gene expression patterns in Zyginidia, even if it is the most conspicuous phenotypic consequence; otherwise, we would expect the three phenotypically female groups (F, FW and MW) to cluster together and the only male group (M) to stand separate from them. None of the PCs show such a pattern. PCA was repeated on expression values without the initial outlier filtering, and applying several different normalization and transformation strategies; they all yielded the same picture as described above: the main effect was invariably the presence or absence of Wolbachia regardless of sex (details not shown).

Bottom Line: Despite the resemblance of Wolbachia-infected chromosomal males to uninfected and infected chromosomal females in terms of sexual morphology and behavior, principal component analysis revealed that gene expression patterns did not follow these sexual phenotype categories.The principal components generated by differentially expressed genes specified a strong sex-independent Wolbachia effect, followed by a weaker Wolbachia-sexual karyotype interaction effect.Approaches to further examine the molecular mechanism of Wolbachia-host interactions have been suggested based on the presented findings.

View Article: PubMed Central - PubMed

Affiliation: Program in Molecular and Computational Biology, Department of Biological Sciences, University of Southern California Los Angeles, CA, USA.

ABSTRACT
Wolbachia causes the feminization of chromosomally male embryos in several species of crustaceans and insects, including the leafhopper Zyginidia pullula. In contrast to the relatively well-established ecological aspects of male feminization (e.g., sex ratio distortion and its consequences), the underlying molecular mechanisms remain understudied and unclear. We embarked on an exploratory study to investigate the extent and nature of Wolbachia's effect on gene expression pattern in Z. pullula. We sequenced whole transcriptomes from Wolbachia-infected and uninfected adults. 18147 loci were assembled de novo, including homologs of several Drosophila sex determination genes. A number of transcripts were flagged as candidate Wolbachia sequences. Despite the resemblance of Wolbachia-infected chromosomal males to uninfected and infected chromosomal females in terms of sexual morphology and behavior, principal component analysis revealed that gene expression patterns did not follow these sexual phenotype categories. The principal components generated by differentially expressed genes specified a strong sex-independent Wolbachia effect, followed by a weaker Wolbachia-sexual karyotype interaction effect. Approaches to further examine the molecular mechanism of Wolbachia-host interactions have been suggested based on the presented findings.

No MeSH data available.


Related in: MedlinePlus